Oxidation of Ingested Phenolics in the Tree-Feeding Caterpillar Orgyia leucostigma Depends on Foliar Chemical Composition

  • Raymond Barbehenn
  • Quentin Weir
  • Juha-Pekka Salminen
Article

Abstract

Tannins are believed to function as antiherbivore defenses, in part, by acting as prooxidants. However, at the high pH found in the midguts of caterpillars, the oxidative activities of different types of tannins vary tremendously: ellagitannins >> galloyl glucoses > condensed tannins. Ingested ascorbate is utilized by caterpillars to minimize phenolic oxidation in the midgut. Thus, leaves that contain higher levels of reactive tannins and lower levels of ascorbate were hypothesized to produce higher levels of phenolic oxidation in caterpillars. We tested this hypothesis with eight species of deciduous trees by measuring their foliar phenolic and ascorbate compositions and measuring the semiquinone radical (oxidized phenolic) levels formed in caterpillars that ingested each species. When the generalist caterpillars of Orgyia leucostigma (Lymantriidae) fed on the leaves of tree species in which condensed tannins were predominant (i.e., Populus tremuloides, P. deltoides, and Ostrya virginiana), semiquinone radical levels were low or entirely absent from the midgut contents. In contrast, species that contained higher levels of ellagitannins (or galloyl rhamnoses; i.e., Quercus alba, Acer rubrum, and A. saccharum) produced the highest levels of semiquinone radicals in O. leucostigma. Low molecular weight phenolics contributed relatively little to the overall oxidative activities of tree leaves compared with reactive tannins. Ascorbate levels were lowest in the species that also contained the highest levels of oxidatively active tannins, potentially exacerbating phenolic oxidation in the gut lumen. We conclude that the tannin compositions of tree leaves largely determine the effectiveness of foliar phenolics as oxidative defenses against caterpillars such as O. leucostigma.

Keywords

Oxidative stress Phenolic oxidation Tannin Semiquinone radical Caterpillar Herbivore Tree chemical defense 

References

  1. Abou-Zaid, M. M., and Nozzolillo, C. 1999. 1-O-galloyl-α-l-rhamnose from Acer rubrum. Phytochemistry 52:1629–1631.CrossRefGoogle Scholar
  2. Abou-Zaid, M. M., Helson, B. V., Nozzolillo, C., and Arnason, J. T. 2001. Ethyl m-digallate from red maple, Acer rubrum L., as the major resistance factor to forest tent caterpillar, Malacosoma disstria Hbn. J. Chem. Ecol. 27:2517–2527.PubMedCrossRefGoogle Scholar
  3. Baker, W. L. 1972. Eastern forest insects. USDA miscellaneous publication no. 1175. Washington, DC.Google Scholar
  4. Barbehenn, R. V. 2001. Roles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals. Arch. Insect Biochem. Physiol. 47:86–99.PubMedCrossRefGoogle Scholar
  5. Barbehenn, R. V. 2003. Antioxidants in grasshoppers: higher levels defend the midgut tissues of a polyphagous species than a graminivorous species. J. Chem. Ecol. 29:683–702.PubMedCrossRefGoogle Scholar
  6. Barbehenn, R. V., Bumgarner, S. L., Roosen, E., and Martin, M. M. 2001. Antioxidant defenses in caterpillars: role of the ascorbate recycling system in the midgut lumen. J. Insect Physiol. 47:349–357.PubMedCrossRefGoogle Scholar
  7. Barbehenn, R. V., Walker, A. C., and Uddin, F. 2003a. Antioxidants in the midgut fluids of a tannin-tolerant and a tannin-sensitive caterpillar: effects of seasonal changes in tree leaves. J. Chem. Ecol. 29:1099–1116.PubMedCrossRefGoogle Scholar
  8. Barbehenn, R. V., Poopat, U., and Spencer, B. 2003b. Semiquinone and ascorbyl radicals in the gut fluids of caterpillars measured with EPR spectrometry. Insect Biochem. Mol. Biol. 33:125–130.PubMedCrossRefGoogle Scholar
  9. Barbehenn, R. V., Cheek, S., Gasperut, A., Lister, E., and Maben, R. 2005. Phenolic compounds in red oak and sugar maple leaves have prooxidant activities in the midguts of Malacosoma disstria and Orgyia leucostigma caterpillars. J. Chem. Ecol. 31:969–988.PubMedCrossRefGoogle Scholar
  10. Barbehenn, R. V., Jones, C. P., Karonen, M., and Salminen, J.-P. 2006a. Tannin composition affects the oxidative activities of tree leaves. J. Chem. Ecol. 32:2235–2251.PubMedCrossRefGoogle Scholar
  11. Barbehenn, R. V., Jones, C. P., Hagerman, A. E., Karonen, M., and Salminen, J.-P. 2006b. Ellagitannins have greater oxidative activities than gallotannins and condensed tannins at high pH: potential impact on caterpillars. J. Chem. Ecol. 32:2253–2267.PubMedCrossRefGoogle Scholar
  12. Barbosa, P., and Krischik, V. A. 1987. Influence of alkaloids on feeding preference of eastern deciduous forest trees by the gypsy moth Lymantria dispar. Amer. Nat. 130:53–69.CrossRefGoogle Scholar
  13. Bi, J. L., and Felton, G. W. 1995. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J. Chem. Ecol. 21:1511–1530.CrossRefGoogle Scholar
  14. Bi, J. L., Murphy, J. B., and Felton, G. W. 1997. Antinutritive and oxidative components as mechanisms of induced resistance in cotton. J. Chem. Ecol. 23:97–117.CrossRefGoogle Scholar
  15. Clausen, T. P., Reichardt, P. B., Bryant, J. P., Werner, R. A., Post, K., and Frisby, K. 1989. Chemical model for short-term induction in quaking aspen (Populus tremuloides) foliage against herbivores. J. Chem. Ecol. 15:2335–2346.CrossRefGoogle Scholar
  16. Felton, G. W., and Duffey, S. S. 1992. Ascorbate oxidation reduction in Helicoverpa zea as a scavenging system against dietary oxidants. Arch. Insect Biochem. Physiol. 19:27–37.CrossRefGoogle Scholar
  17. Gant, T. W., Ramakrishna, R., Mason, R. P., and Cohen, G. M. 1988. Redox cycling and sulphydryl arylation; their relative importance in the mechanism of quinone cytotoxicity to isolated hepatocytes. Chem.-Biol. Interactions 65:157–173.CrossRefGoogle Scholar
  18. Haruta, M., Pedersen, J. A., and Constabel, P. 2001. Polyphenol oxidase and herbivore defense in trembling aspen (Populus tremuloides): cDNA cloning, expression, and potential substrates. Physiol. Plant 112:552–558.PubMedCrossRefGoogle Scholar
  19. Hemming, J. D. C., and Lindroth, R. L. 1995. Intraspecific variation in aspen phytochemistry: Effects on performance of gypsy moths and forest tent caterpillars. Oecologia 103:79–88.CrossRefGoogle Scholar
  20. Hofmann, A. S., and Gross, G. G. 1990. Biosynthesis of gallotannins: Formation of polygalloylglucoses by enzymatic acylation of 1,2,3,4,6-penta-O-galloylglucose. Arch. Biochem. Biophys. 283:530–532.PubMedCrossRefGoogle Scholar
  21. Johnson, K. S., and Felton, G. W. 2001. Plant phenolics as dietary antioxidants for herbivorous insects: A test with genetically modified tobacco. J. Chem. Ecol. 27:2579–2597.PubMedCrossRefGoogle Scholar
  22. Liebhold, A. M., Gottschalk, K. W., Muzika, R.-M., Montgomery, M. E., Young, R., O’Day, K., and Kelley, B. 1995. Suitability of North American tree species to the gypsy moth: a summary of field and laboratory tests. USDA Forest Service, General Technical Report NE-211.Google Scholar
  23. Lindroth, R. L., and Peterson, S. S. 1988. Effects of plant phenols on performance of southern armyworm larvae. Oecologia 75:185–189.CrossRefGoogle Scholar
  24. Lindroth, R. L., Hsia, M. T. S., and Scriber, J. M. 1987. Seasonal patterns in the phytochemistry of three Populus species. Biochem. Syst. Ecol. 15:681–686.CrossRefGoogle Scholar
  25. Martin, J. S., Martin, M. M., and Bernays, E. A. 1987. Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: implications for theories of plant defense. J. Chem. Ecol. 13:605–621.CrossRefGoogle Scholar
  26. Moilanen, J., and Salminen, J.-P. 2008. Ecologically neglected tannins and their biologically relevant activity: chemical structures of plant ellagitannins reveal their in vitro oxidative activity at high pH. Chemoecology, (in press).Google Scholar
  27. Ossipova, S., Ossipov, V., Haukioja, E., Loponen, J., and Pihlaja, K. 2001. Proanthocyanidins of mountain birch leaves: quantification and properties. Phytochem. Anal. 12:128–133.PubMedCrossRefGoogle Scholar
  28. Parry, D., and Goyer, R. A. 2004. Variation in the suitability of host tree species for geographically discrete populations of forest tent caterpillar. Environ. Entomol. 33:1477–1487.CrossRefGoogle Scholar
  29. Rosen, G. M., Britigan, B. E., Halpern, H. J., and Pou, S. 1999. Free Radicals: Biology and Detection by Spin Trapping. Oxford University Press, NY.Google Scholar
  30. Ruuhola, T., Tikkanen, O.-P., and Tahvanainen, J. 2001. Differences in host use efficiency of larvae of a generalist moth, Operophtera brumata on three chemically divergent Salix species. J. Chem. Ecol. 27:1595–1615.PubMedCrossRefGoogle Scholar
  31. Salminen, J.-P., Ossipov, V., Loponen, J., Haukioja, E., and Pihlaja, K. 1999. Characterisation of hydrolyzable tannins from leaves of Betula pubescens by high-performance liquid chromatography-mass spectrometry. J. Chrom. A. 864:283–291.CrossRefGoogle Scholar
  32. Sas institute 2003. The SAS system for Windows. Version 9.1. SAS Institute, Cary, NC, USA.Google Scholar
  33. Summers, C. B., and Felton, G. W. 1994. Prooxidant effects of phenolic acids on the generalist herbivore Helicoverpa zea (Lepidoptera: Noctuidae): Potential mode of action for phenolic compounds in plant anti-herbivore chemistry. Insect Biochem. Mol. Biol. 24:943–953.CrossRefGoogle Scholar
  34. Thiboldeaux, R. L., Lindroth, R. L., and Tracy, J. W. 1998. Effects of juglone (5-hydroxy-1,4-naphthoquinone) on midgut morphology and glutathione status in Saturniid moth larvae. Comp. Biochem. Physiol. 120:481–487.Google Scholar
  35. Wagner, D. M. 2005. Caterpillars of Eastern North America. Princeton University Press.Google Scholar
  36. Wilkinson, L. 2000. SYSTAT: The system for statistics. SYSTAT, Inc., Evanston, IL.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Raymond Barbehenn
    • 1
  • Quentin Weir
    • 1
  • Juha-Pekka Salminen
    • 2
  1. 1.Departments of Molecular, Cellular and Developmental Biology and Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA
  2. 2.Laboratory of Organic Chemistry and Chemical Biology, Department of ChemistryUniversity of TurkuTurkuFinland

Personalised recommendations